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Fluorene Exposure Among PAH-Exposed Workers Is Exposure assessment Occup Environ Med: first published as 10.1136/oemed-2020-106413 on 8 May 2020. Downloaded from ORIGINAL RESEARCH Fluorene exposure among PAH- exposed workers is associated with epigenetic markers related to lung cancer Ayman Alhamdow ,1 Yona J Essig,2 Annette M Krais,2 Per Gustavsson ,1,3 Håkan Tinnerberg,4 Christian H Lindh,2 Jessika Hagberg,5,6 Pål Graff ,7 Maria Albin,1,2,3 Karin Broberg 1,2 ► Additional material is ABSTRact Key messages published online only. To view Objectives Exposure to high- molecular- weight please visit the journal online polycyclic aromatic hydrocarbons (PAHs) may cause (http:// dx. doi. org/ 10. 1136/ What is already known about this subject? cancer in chimney sweeps and creosote-exposed workers, oemed- 2020- 106413). Occupational exposure to high- molecular- however, knowledge about exposure to low- molecular- ► weight polycyclic aromatic hydrocarbons (PAHs) For numbered affiliations see weight PAHs in relation to cancer risk is limited. In this has been widely studied in relation to cancer end of article. study, we aimed to investigate occupational exposure biomarkers, however, less is known about to the low- molecular- weight PAHs phenanthrene and Correspondence to exposure to low- molecular- weight PAHs and fluorene in relation to different cancer biomarkers. Dr Karin Broberg, Institute their carcinogenicity. of Environmental Medicine, Methods We recruited 151 chimney sweeps, 19 ► Workers exposed to PAHs are at a higher risk of Karolinska Institutet, Stockholm creosote- exposed workers and 152 unexposed workers cancer. SE-171 76, Sweden; (controls), all men. We measured monohydroxylated Hypomethylation of F2RL3 and AHRR has been karin. broberg@ ki. se metabolites of phenanthrene and fluorene in urine ► shown to be marker for lung cancer risk. AA and YJE contributed equally. using liquid chromatography coupled to tandem mass spectrometry. We measured, in peripheral blood, the What are the new findings? Received 9 January 2020 cancer biomarkers telomere length and mitochondrial ► Chimney sweeps and creosote- exposed workers Revised 2 April 2020 DNA copy number using quantitative PCR; and DNA Accepted 5 April 2020 were exposed to the low-molecular -weight methylation of F2RL3 and AHRR using pyrosequencing. PAHs fluorene and phenanthrene. Results Median PAH metabolite concentrations ► Fluorene exposure was associated with the were higher among chimney sweeps (up to 3 times) hypomethylation of F2RL3 and AHRR. and creosote- exposed workers (up to 353 times), compared with controls (p<0.001; adjusted for age How might this impact policy or clinical prac- http://oem.bmj.com/ and smoking). ∑OH- fluorene (sum of 2- hydroxyfluorene tice in the foreseeable future? and 3- hydroxyfluorene) showed inverse associations ► This study highlights the importance of with percentage DNA methylation of F2RL3 and AHRR measuring not only high-molecular -weight PAHs in chimney sweeps (B (95% CI)=–2.7 (–3.9 to –1.5) but also the low- molecular- weight PAHs when for F2RL3_cg03636183, and –7.1 (–9.6 to –4.7) for assessing occupational PAH exposure. AHRR_cg05575921: adjusted for age and smoking), but ► Further, it indicates that even exposure to not in creosote- exposed workers. In addition, ∑OH- low-molecular -weight PAHs might have a on September 27, 2021 by guest. Protected copyright. fluorene showed a 42% mediation effect on the inverse carcinogenic effect. If this is the case, then the association between being a chimney sweep and DNA number of workers under risk is much larger methylation of AHRR CpG2. than currently assumed, as many workers are Conclusions Chimney sweeps and creosote-exposed exposed to low-molecular -weight PAHs only. workers were occupationally exposed to low- molecular- weight PAHs. Increasing fluorene exposure, among chimney sweeps, was associated with lower DNA Finland, Denmark and Iceland).2 For instance, methylation of F2RL3 and AHRR, markers for increased standardised incidence ratio (SIR) and 95% CI for lung cancer risk. These findings warrant further chimney sweeps in all countries were SIR 2.41 investigation of fluorene exposure and toxicity. (95% CI: 1.40 to 3.85) for pharynx cancer, and SIR 1.86 (95% CI: 1.19 to 2.76) for oesophageal © Author(s) (or their cancer.2 Moreover, high risk for cancer was seen in employer(s)) 2020. Re- use permitted under CC BY. a cohort of chimney sweeps (n=6320) from Sweden Published by BMJ. INTRODUCTION (eg, SIR=1.30 (95% CI: 1.21 to 1.39) for total Scrotal cancer among chimney sweeps was the cancer; and SIR=2.08 (95% CI: 1.19 to 3.38) for To cite: Alhamdow A, 1 3 first cancer form linked to chemical exposure. oesophageal cancer). The same study found that Essig YJ, Krais AM, et al. Occup Environ Med Epub Even today, the risk of occupational cancer among the number of working years as a chimney sweep (a ahead of print: [please include chimney sweeps is very high, based on analysis of proxy for soot exposure) was positively associated Day Month Year]. doi:10.1136/ 53 occupational groups (n=15 million individ- with cancer incidence.3 The major carcinogenic oemed-2020-106413 uals) from the Nordic countries (Sweden, Norway, exposure for the chimney sweeps is considered to Alhamdow A, et al. Occup Environ Med 2020;0:1–8. doi:10.1136/oemed-2020-106413 1 Exposure assessment Occup Environ Med: first published as 10.1136/oemed-2020-106413 on 8 May 2020. Downloaded from be polycyclic aromatic hydrocarbons (PAHs)—the main constit- for controls, and on Thursdays for creosote- exposed workers, uent of soot.4 5 The International Agency for Research on Cancer during which trained nurses collected questionnaires, sampled (IARC) has classified PAHs as human carcinogens (group 1: eg, blood and urine, and measured weight and height. The ques- benzo[a]pyrene; BaP), probable human carcinogens (group 2A: tionnaire included questions about age, chronic diseases, level eg, dibenz[a,h]anthracene), possible human carcinogens (group of education, tobacco smoking history, intake of dietary items 2B: eg, benz[a]anthracene; BaA) or not classifiable as to their including vegetables, fruits and fish, use of chewing tobacco carcinogenicity to humans (group 3: eg, pyrene, phenanthrene (snus), passive smoking, physical activity, residential history, (Phe) and fluorene (Flu)).6 Creosote- impregnating workers is employment history and exposure from hobbies. The question- another occupational group exposed to PAHs with an elevated naire of chimney sweeps further explored the extent of workers’ risk for cancer.6 7 Workers in this occupation are exposed to engagement in different sweeping tasks (eg, soot sweeping in PAHs from creosote oil, which is classified as a probable human private houses as well as in industrial buildings) during different carcinogen.6 time periods (eg, during the past 12 months). We previously demonstrated, by measuring four PAH metab- Postshift spot urine and EDTA blood samples were collected olites in urine, that currently working chimney sweeps and from participants and transported at room temperature to the creosote- exposed workers in Sweden were exposed to the Division of Occupational and Environmental Medicine, Lund PAHs pyrene and phenanthrene, BaA and BaP (BaP was only University for storage at −20°C. Five chimney sweeps and four found in chimney sweeps).4 8 Notably, the highest PAH expo- controls refrained from donating blood samples, whereas three sure, measured as urinary PAH metabolites, found in creosote- chimney sweeps and one control could not urinate. All creosote- exposed workers was phenanthrene—a low- molecular- weight exposed workers donated blood and urine samples. Written PAH (median 2- OH- phenanthrene concentrations in urine were informed consent was obtained from all study participants. The 29.6 vs 0.14 µg/g creatinine for creosote- exposed workers and study was carried out in accordance with the ethical guidelines controls, respectively). Phenanthrene and other low- molecular- of the Declaration of Helsinki 1964 and its later amendments weight PAHs, such as fluorene, might thus be interesting and was approved by the Regional Ethics Committee in Lund, targets for biomonitoring studies of PAH- exposed workers. We Sweden and the Regional Ethics Committee in Uppsala, Sweden. also showed that both chimney sweeps and creosote- exposed workers had lower DNA methylation of the genes F2RL3 and PAH metabolites in urine AHRR—prospective biomarkers for lung cancer.8 9 We did not We measured urinary monohydroxylated metabolites of phenan- find any associations with relative telomere length (TL) or threne (1- OH- Phe, 2- OH- Phe, 3- OH- Phe and 4- OH- Phe) and mitochondrial DNA copy number (mtDNAcn), two biomarkers fluorene (2- OH-Flu and 3- OH-Flu) by liquid chromatography previously linked to cancer risk,10 11 nor did we observe associ- coupled to tandem mass spectrometry (LC-MS/MS). Details of ations between the four measured PAH metabolites and DNA the method were described previously.4 Urine samples (0.2 mL) methylation levels.8 The latter observation may be due to differ- were pipetted into a 96-well plate and hydrolysed by adding ences in half- lives between the urinary PAH metabolites and 0.1 mL of ammonium acetate (pH 6.5) and 0.01 mL of β-glucuro- DNA methylation, or alternatively, that the four PAHs analysed nidase (Escherichia coli). The solution was incubated for 30 min do not cause epigenetic changes. It therefore remains to clarify at 37°C. Afterwards, 0.025 mL of a 50:50 (v/v) water/acetonitrile if PAHs present in soot and creosote oil can cause the cancer- solution and 0.025 mL of deuterium- labelled internal standards related DNA methylation. This will increase our knowledge of http://oem.bmj.com/ (D -1- OH- Phe, D -2- OH- Phe, D -4- OH- Phe, D -2- OH- Flu; occupational PAH exposure and related risk of cancer. 9 9 9 9 Toronto Research Chemicals, North York, Ontario, Canada) We aimed in this study to (i) further characterise the expo- were added (final concentrations 5 ng/mL).
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